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Variability in Diel and Seasonal in Situ Metabolism of the Tropical Gastropod Tectus Niloticus

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Variability in Diel and Seasonal in Situ Metabolism of the Tropical Gastropod Tectus Niloticus Vol. 23: 167–182, 2015 AQUATIC BIOLOGY Published online February 11 doi: 10.3354/ab00618 Aquat Biol OPENPEN ACCESSCCESS Variability in diel and seasonal in situ metabolism of the tropical gastropod Tectus niloticus A. Lorrain1,*, J. Clavier2, J. Thébault2, L. Tremblay-Boyer3, F. Houlbrèque4, E. Amice2, M. Le Goff2, L. Chauvaud2 1IRD, Laboratoire des Sciences de l’Environnement Marin (UMR 6539 CNRS/UBO/IRD/IFREMER), BP A5, 98848 Nouméa cedex, New Caledonia, France 2Université de Brest, Institut Universitaire Européen de la Mer, Laboratoire des Sciences de l’Environnement Marin (UMR 6539 CNRS/UBO/IRD/IFREMER), 29280 Plouzané, France 3Biodiversity Centre, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada 4IRD, UR CoRéUs 2, BP A5, 98848 Nouméa cedex, New Caledonia, France ABSTRACT: Researchers often use metabolic measurements in the field over narrow time periods to estimate an organism’s metabolism over large time scales. Here, we measured in situ respira- tion, calcification and excretion rates of the tropical gastropod Tectus niloticus L. through benthic chamber experiments. Our samples spanned a 21 h time frame and were taken during both the warm and cool seasons. We assessed diel and seasonal variability in metabolic rates, as well as the effect of individual size and the contribution of shell epi- and endobionts. Our results show that metabolic rates vary through time at both diel and seasonal scales, as measured fluxes for respira- tion and calcification were significantly higher at night during the warm season. This nocturnal pattern was not significant in the cool season. Size effects were significant with higher respiration and calcification rates for small individuals regardless of the season, although the difference tended to be more pronounced in the warm season. We also found that shell epi- and endobionts made an important contribution to respiration, as 40 and up to 100% of total measured fluxes for night and day, respectively, could be attributed to the shell community. More importantly, the direction of the measured flux was occasionally opposite that of the individual trochus, highlight- ing that the contribution of shell epi- and endobionts must be accounted for in order to achieve an accurate understanding of individual metabolism. Lastly, depending on the time of day and season when measurements are taken, ignoring diel or seasonal variations in metabolic rates could result in important under- or overestimation of the contributions of gastropods to carbon and calcium carbonate fluxes in coastal ecosystems. KEY WORDS: Gastropod · Seasonal variations · Diel variations · Size · Carbon fluxes · CO2 · CaCO3 · New Caledonia INTRODUCTION empirically through oxygen respiratory fluxes con- verted to carbon using available respiratory quotients Respiration and biocalcification of marine animals (Boucher & Clavier 1995) or by directly assessing car- such as molluscs can be a source of CO2 into the eco- bon metabolism through respiration and calcification system and their role in the carbon cycle has been measurements (e.g. Martin et al. 2006). While most demonstrated in temperate environments (Chauvaud studies have focused on temperate molluscs, either to et al. 2003, Clavier et al. 2009, Lejart et al. 2012, Mis- infer their role in the carbon cycle (Martin et al. 2006, tri & Munari 2013). This contribution can be assessed Lejart & Hily 2011, Lejart et al. 2012, Mistri & Munari © The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 168 Aquat Biol 23: 167–182, 2015 2013) or to gain better insight into their adaptive algae, encrusting calcareous algae and endo lithic strategies (Tagliarolo et al. 2012, 2013a,b), few studies flora (Heisterkamp et al. 2013). Until now, the influ- are available for tropical molluscs (but see Boucher- ence of these epi- and endobionts on respiration and Rodoni & Boucher 1993). calcification in molluscs has never been considered. Tectus niloticus L. is a large tropical marine snail The objectives of this study were therefore to (1) esti- commonly known as topshell or trochus. The species mate in situ diel variations of trochus underwater res- is widespread throughout Southeast Asia and the piration and calcification in a tropical ecosystem, (2) Western Pacific, and has been introduced in many test the influence of individual size and seasons on South Pacific islands (Purcell & Cheng 2010). Trochus the corresponding carbon, calcium carbonate and meat is a source of protein, while its shells have been ammonium fluxes, and (3) determine if shell epi- and traditionally used for ornaments by indigenous peo- endobionts have a significant impact on these differ- ple (Castell & Sweatman 1997, Hoang et al. 2008). ent fluxes. This species is also one of the most valuable and sought-after reef gastropods because its shell can be used in the manufacture of mother-of-pearl buttons MATERIALS AND METHODS (Castell & Sweatman 1997), which can be a valuable source of income for people in the Indo-Pacific re - Study site gion. However, overharvesting is causing a rapid de - cline in its numbers (Nash 1993, Castell 1997, Castell Field work was conducted from the RV ‘Alis’ in the & Sweatman 1997). Because of commercial interest southwest New Caledonian lagoon on the Tabou reef and the risk of overfishing, this species has been (22° 28.861’ S; 166° 26.793’ E; Fig. 1) on 4−5 February the subject of numerous biological studies (e.g. Bour (warm season) and 23−24 August 2012 (cool season), 1989, Castell & Sweatman 1997, Pakoa et al. 2010, to sample 2 seasons with contrasting temperatures. Purcell & Cheng 2010). In this region, lower water temperatures occur dur- Trochus can be found in both intertidal and sub- ing the cool season from May to November while tidal reef areas, generally in high energy sections of high water temperatures are seen in January and the reef (Bour 1990, Pakoa et al. 2010). While the February (22.3 vs. 28.1°C; Clavier & Garrigue 1999). optimum depth for T. niloticus is between 0 and 15 m, Trochus individuals were harvested by SCUBA divers individuals can be found as deep as 25 m (Pakoa et at between 2 and 7 m depth at the Amédée reef al. 2010). Juveniles are quite cryptic but larger indi- (22° 28.804’ S; 166° 27.877’ E; Fig. 1), where the highest viduals are found easily on tropical coral reef flats average density occurs for this species in New Cale- (Castell 1997). T. niloticus has a large, thick shell and donia (0.69 ± 0.43 ind. m−2; P. Dumas pers. comm.). can grow to over 15 cm (basal diameter). Typical life- Specimens were then transferred to the study site at span is 15 to 20 yr, and reproductive maturity is a depth of 7 m in February, and 3 m in August. Sea reached after 2 yr and at a basal diameter of ca. 6 cm temperatures for the Amédée reef station (Fig. 1) were (Castell 1997). Trochus are herbivores and tend to eat obtained at 30 min intervals via a Seabird SBE56 turf algae and biofilm by grazing on corals and rocks from the ReefTEMPS network (http:// webgops. ird. (Villanueva et al. 2013). They are mainly nocturnal nc/ geoserver/www/reeftemps_network.html). (Bour 1989), with feeding rates increasing signifi- cantly at night (Heslinga & Hillmann 1981). Together with the objective of increasing general Incubation protocol knowledge of an exploited tropical gastropod, ex- amining trochus diel activity patterns provide an Dissolved inorganic carbon (DIC) and calcium car- excellent opportunity to consider variations of carbon bonate (CaCO3) fluxes associated with Tectus niloti- metabolism over a 24 h cycle. Variations in res pira - cus were measured in situ using transparent Plexi- tion or calcification of marine organisms have al - glas benthic chambers 0.19 m in diameter (Fig. 2). ready been measured over different seasons (Lejart The enclosed volume ranged from 6.3 to 6.9 l et al. 2012), but diel variations are rarely considered (depending on the exact length of hoses connecting since measurements tend to be taken only during the the different parts of the experimental system and on day, even for large-scale extrapolations of carbon trochus volume). Once during the warm and the cool metabolism. Furthermore, trochus shells, similar to season, 4 chambers were deployed simultaneously carbonate substrates (Tribollet 2008), are colonized and a series of 8 incubations with the same speci- by epi- and endobionts such as bacterial biofilm, turf mens were performed over a 24 h period to encom- Lorrain et al.: Variability in Tectus niloticus metabolism 169 164°E 165°E 166°E 167°E 22°10’ 20°S S 21°S 22°S NOUMÉA Pacific Ocean 23°S 22°20’ Barrier reef Tabou reef 22°30’ Amédée N reef Land Reef S 166°10’E 166°20’ 166°30’ 166°40’ Fig. 1. Sampling site for Tectus niloticus metabolism measurements (Tabou reef) and environmental survey (Amédée reef) in the southwest lagoon of New Caledonia pass the full range of daily irradiance levels. Each of these incubations was carried out for 1 h. The enclo- sures were then opened for at least 30 min between subsequent incubations to restore ambient condi- tions in the chamber. Adjustable submersible pumps connected to waterproof batteries mixed the water 3 inside the enclosures at a water flow rate of 2 l min−1 (see Fig. 2). To assess the effect of animal size on fluxes, the chambers contained either small trochus (max. basal diameter 51 to 75 mm) or large trochus 1 (112 to 121 mm) (2 chambers per size treatment). The 2 small size treatment chambers contained 4 small 4 5 trochus and the large size treatment chambers con- tained one large trochus to maintain the same amount of total biomass in each benthic chamber.
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